How multiple mating by females affects sexual selection

Multiple mating by females is widely thought to encourage post-mating sexual selection and enhance female fitness. We show that whether polyandrous mating has these effects depends on two conditions. Condition 1 is the pattern of sperm utilization by females; specifically, whether, among females, male mating number, m (i.e. the number of times a male mates with one or more females) covaries with male offspring number, o. Polyandrous mating enhances sexual selection only when males who are successful at multiple mating also sire most or all of each of their mates'' offspring, i.e. only when Cov_♂(m,o), is positive. Condition 2 is the pattern of female reproductive life-history; specifically, whether female mating number, m, covaries with female offspring number, o. Only semelparity does not erode sexual selection, whereas iteroparity (i.e. when Cov_♀(m,o), is positive) always increases the variance in offspring numbers among females, which always decreases the intensity of sexual selection on males. To document the covariance between mating number and offspring number for each sex, it is necessary to assign progeny to all parents, as well as identify mating and non-mating individuals. To document significant fitness gains by females through iteroparity, it is necessary to determine the relative magnitudes of male as well as female contributions to the total variance in relative fitness. We show how such data can be collected, how often they are collected, and we explain the circumstances in which selection favouring multiple mating by females can be strong or weak.     

Female mating frequency in a wild population of scorpionflies (Panorpa germanica, Panorpidae, Mecoptera)

In this study, we investigated mating frequencies of female scorpionflies Panorpa germanica in the field using two different experimental approaches. First, the mating status of wild‐caught females was estimated on the basis of sperm numbers present inside their sperm storage organs. Secondly, the number of mating partners wild‐caught females must have had was inferred from mother‐offspring analyses of a polymorphic microsatellite locus. Our results suggest a very low mating frequency of wild female P. germanica. Consequently, the risk of sperm competition is rather low in this species. The relevance of female mate choice in relation to the low mating frequency is discussed.     

Implications of multiple mating for offspring relatedness and shoaling behaviour in juvenile guppies

Polyandry (female multiple mating) can confer important benefits to females, but few studies have considered its potential costs. One such cost may arise through differences in the relatedness of offspring born to females with different mating histories; offspring born to monandrous females are always full siblings, while those produced by polyandrous females may be full or half siblings. These differences may have important consequences for social interactions among offspring. We used artificial insemination in the guppy (Poecilia reticulata), a promiscuous live-bearing fish, to evaluate shoaling behaviour in polyandrous and monandrous broods. We combined this information with known parentage data for the polyandrous broods to determine whether sibling relatedness influenced offspring shoaling behaviour. While we detected no effect of mating treatment (polyandry/monandry) on shoaling behaviour, we found that pairs of full siblings spent significantly more time shoaling (and in close proximity) than pairs of half siblings. This latter finding confirms the ability of newborn guppies to distinguish brood mates on the basis of kinship, but also suggests an important and hitherto unrealized potential cost of polyandry: a reduction in within-brood relatedness with potentially important implications for offspring social behaviour.     

Coevolution of male and female reproductive traits in a simultaneously hermaphroditic land snail

Inter- and intraspecific studies in gonochoristic animals reveal a covariation between sperm characteristics and the size of the female reproductive tract, indicating a rapid evolutionary divergence, which is consistent with the theory of post-copulatory sexual selection. Simultaneous hermaphrodites differ from species with separate sexes (gonochorists) in that they possess both functional male and female reproductive organs at the same time. We investigated whether in hermaphroditic animals intraspecific variation in reproductive traits results from divergent coevolution, by quantifying the variation in male and female traits among six natural populations of the snail Arianta arbustorum and examining the covariation in interacting traits. There was a significant among-population variation in spermatophore volume, number of sperm transferred and sperm length, as well as in volume of the sperm storage organ (spermatheca) and number of tubules, but not in spermatheca length. We found a positive association between sperm number transferred and spermatheca volume. This result suggests that the same post-copulatory mechanisms as in gonochorists drive the correlated evolution of reproductive characters in hermaphrodites.     

Spermicide, cryptic female choice and the evolution of sperm form and function

Sperm competition and cryptic female choice profoundly affect sperm morphology, producing diversity within both species and individuals. One type of within-individual sperm variation is sperm heteromorphism, in which each male produces two or more distinct types of sperm simultaneously, only one of which is typically fertile (the "eusperm"). The adaptive significance of nonfertile "parasperm" types is poorly understood, although numerous sperm-heteromorphic species are known from many disparate taxa. This paper examines in detail two female-centred hypotheses for the evolution and maintenance of this unconventional sperm production strategy. First, we use game theoretical models to establish that parasperm may function to protect eusperm from female-generated spermicide, and to elucidate the predictions of this idea. Second, we expand on the relatively undeveloped idea that parasperm are used by females as a criterion for cryptic female choice, and discuss the predictions generated by this idea compared to other hypotheses proposed to explain sperm heteromorphism. We critically evaluate both hypotheses, suggest ways in which they could be tested, and propose taxa in which they could be important.     

Paternity in mallards: effects of sperm quality and female sperm selection for inbreeding avoidance

Postcopulatory processes might play an important role in sexualselection. In theory, fertilization success could be controlledby females via selection of particular sperm within their reproductivetract, or it could be determined by sperm competition per se.In practice, these two mechanisms are difficult to disentangle.To assess the relative importance of both mechanisms we usedartificial insemination in combination with measurements ofsperm quality (swimming speed and motility) in mallards. Inthis species, females often lack behavioral control over copulationsand hence may use postcopulatory mechanisms to optimize theirreproductive output. One important factor affecting female fitnessmay be selection of genetically compatible males. To investigatethe influence of sperm quality and parental relatedness on paternitywe inseminated 12 groups of related females with a sperm mixturecontaining equal numbers of sperm from a brother and from anunrelated male. Paternity was independent of the relatednessof the siring male to the female but was significantly affectedby long-term sperm swimming speed and motility. No interactionbetween relatedness and sperm quality on paternity was observed.These results suggest that female mallards are not able to selectsperm on a purely genetic basis and emphasize the importanceof sperm quality in gaining paternity.     

Sexual selection in hermit crabs: a review and outlines of future research

The information currently available on sexual selection in hermit crabs is reviewed to identify the role of males and females before, during and after mating. According to this information, possible mechanisms of male–male competition, female choice and/or sexual conflict are suggested. Important male components that may affect mating success include dragging the female shell, rotations of the female's shell and male cheliped palpations, and male size and/or shell characteristics (species and size). Possible female determinants of male mating/fertilization success include size (as an indicator of egg production capacity), signalling of sexual receptivity to males, delay from mate guarding to copulation and mating duration. Avenues for deeper exploration in males include the role of the number and morphometry of male sexual tubes during sperm transfer, and whether ejaculate size and sperm number can be adjusted with variable situations of sperm competition intensity and risk. In females it would be interesting to investigate the chemical and behavioural mechanisms affecting spermatophore breakage for sperm release and the variable duration from sperm transfer to spawning. Given these possibilities, and that sperm is externally deposited on the female's body but inside her shell (except for those species that do not use shells, e.g. Birgus , or species where shells are rather small and do not cover the body totally, e.g. Parapagurus ), we conclude that hermit crabs are unique subjects for separating male and female effects, particularly with respect to the applicability of current ideas in sexual selection such as female choice and sexual conflict. Some practical ideas are provided to disentangle both hypotheses using these animals.     

Interspecific variation in ejaculate allocation and associated effects on female fitness in seed beetles

When ejaculates are costly to produce, males are expected to allocate their ejaculate resources over successive matings in a manner that optimizes their reproductive success and this may have important consequences for their mates. In seed beetles (Coleoptera; Bruchidae), ejaculates vary in size across species from weighing less than 1%, up to as much as 8%, of male body weight. Ejaculates contain not only sperm but also a range of additional substances and females in some species gain benefits from receiving large ejaculates. Male ejaculate allocation may thus affect female fitness. Here, we first characterized the pattern of male ejaculate allocation over successive matings in seven-seed beetle species. We then assessed how this allocation affected female fitness in each species. Although females generally benefited from receiving large ejaculates, the interspecific variation observed both in ejaculate allocation patterns and in their effects on female fitness was remarkably large considering that the species studied are closely related. Our analyses suggest that variation in ejaculate composition is the key, both within and across species. We discuss possible causes for this variation and conclude that coevolution between male ejaculates and female utilization of ejaculate substances has apparently been rapid in this clade.     

Co-evolution of male and female reproductive characters across the Scathophagidae (Diptera)

Sperm morphometry is extremely variable across species, but a general adaptive explanation for this diversity is lacking. As sperm must function within the female, variation in sperm form may be associated with variation in female reproductive tract morphology. We investigated this and other potential evolutionary associations between male and female reproductive characters across the Scathophagidae. Sperm length was positively associated with the length of the spermathecal (sperm store) ducts, indicating correlated evolution between the two. No association was found between sperm length and spermathecal size. However, the size of the spermathecae was positively associated with testis size indicating co-evolution between male investment in sperm production and female sperm storage capacity. Furthermore, species with a higher degree of polyandry (larger testes) had longer spermathecal ducts. However, no associations between sperm length or length variation and testis size were found which suggests greater sperm competition sensu stricto does not select for longer sperm.     

Primate copulation calls and postcopulatory female choice

Females in some species of Old World monkeys and apes vocalizeafter copulation, but the function of these vocalizations isnot clear. In this article, we examine the hypothesis that copulationcalls are a form of postcopulatory female choice. Accordingto this hypothesis, copulation calls are honest signals of fertility(i.e., ovulation) that are used by females to encourage mateguarding by their preferred mating partners and reduce the likelihoodof sperm competition. Evidence in favor of this hypothesis isreviewed and discussed in relation to other hypotheses. We suggestthat the evolution of female copulation calls in primates islinked to the evolution of other female mating signals suchas exaggerated sexual swellings, the potential for sperm competition,and the opportunity for precopulatory female mate choice.     

Males with high genetic similarity to females sire more offspring in sperm competition in Peron's tree frog Litoria peronii

Recent work has confirmed that genetic compatibility among mates can be an important determinant of siring success in sperm competition experiments and in free-ranging populations. Most of this work points towards mate choice of less related mates. However, there may also be the potential for mate choice for intermediate or even genetically similar mates to prevent outbreeding depression or hybridization with closely related taxa. We studied relatedness effects on post-copulatory gametic choice and/or sperm competition in an external fertilizer, Peron's tree frog (Litoria peronii), since external fertilizers offer exceptional control in order to test gametic interaction effects on probability of paternity and zygote viability. Sperm competition experiments were done blindly with respect to genetic relatedness among males and females. Thereafter, paternity of offspring was assigned using eight microsatellite loci. Three hybridization trials between L. peronii and a closely related sympatric species Litoria tyleri were also carried out. In the sperm competition trials, males that are more genetically similar to the female achieved higher siring success compared with less genetically similar males. The hybridization trials confirmed that the two species can interbreed and we suggest that the risk of hybridization may contribute to selection benefits for genetically more similar males at fertilization. To our knowledge, this study is the first to show evidence for post-copulatory selection of sperm from genetically more similar individuals within a natural population.     

The effect of cryptic female choice on sex allocation in simultaneous hermaphrodites

Sex allocation theory for simultaneous hermaphrodites has focused primarily on the effects of sperm competition, but the role of mate choice has so far been neglected. We present a model to study the coevolution of cryptic female choice and sex allocation in simultaneous hermaphrodites. We show that the mechanism of cryptic female choice has a strong effect on the evolutionary outcome: if individuals remove a fixed proportion of less-preferred sperm, the optimal sex allocation is more female biased (i.e. more biased towards egg production) than without cryptic female choice; conversely, if a fixed amount of sperm is removed, sex allocation is less female-biased than without cryptic female choice, and can easily become male biased (i.e. biased towards sperm production). Under male-biased sex allocation, hermaphroditism can become unstable and the population can split into pure males and hermaphrodites with a female-biased allocation. We discuss the idea that the evolution of sex allocation may depend on the outcome of sexual conflict over the fate of received sperm: the sperm donor may attempt to manipulate or by-pass cryptic female choice and the sperm recipient is expected to resist such manipulation. We conclude that cryptic female choice can have a strong influence on sex allocation in simultaneous hermaphrodites and strongly encourage empirical work on this question.     

Independent effects of familiarity and mating preferences for ornamental traits on mating decisions in guppies

The avoidance of familiar individuals as mates can act to maximizethe benefits of polyandry or might help to minimize inbreedingin small or highly philopatric populations. As previous matesare also familiar, the effects of familiarity and mating historycan often be confounded. Here, we disentangle these effectson mating decisions in the guppy, Poecilia reticulata, and examinetheir influence on sexual selection. In 3 experiments, malesand females were 1) able to mate, 2) had visual and olfactorycontact, or 3) had visual contact only. Familiarity was successfullyacquired via visual cues, and females were in all cases morelikely to mate with unfamiliar than with familiar males, indicatingthat familiarity is a more important determinant of mating outcomethan mating history. Males did not court unfamiliar femalesany more than familiar females and did not differentially allocatesperm. Familiarity did not alter the strength of sexual selectionon male coloration: we found overall positive selection forbright, large males. Female preferences for unfamiliar malesand ornamental traits may therefore be largely independent.     

Effects of Sexual Selection Upon Sperm Morphology and Sexual Skin Morphology in Primates

We review possible effects of sexual selection upon sperm morphology, and sexual skin morphology, in primates. Comparative morphometric studies, involving 31 species representing 21 primate genera, revealed a positive relationship between volume of the sperm midpiece, occurrences of multiple partner matings by females, and large relative testes sizes, which indicate sperm competition. The midpiece houses the mitochondria required to power sperm motility. Hence, sperm competition may have influenced the evolution of increased mitochondrial loading in species where females mate with multiple partners during the fertile period. Females of some Old World monkey species and female chimpanzees exhibit large estrogen-dependent sexual skin swellings during the follicular phase of the menstrual cycle. Studies of mandrills support the conclusion that swellings act primarily as sexually attractive, graded signals and that swelling size may indicate current reproductive quality. Measurements of the genitalia in chimpanzees indicate a secondary function for female swellings. The swelling increases the operating depth of the female's vagina by 50% during the fertile phase of her cycle. Males have evolved long, filiform penes capable of placing sperm close to the os cervix during competitive multipartner matings. This may exemplify how morphologic specializations in females can influence the coevolution of advantageous genitalic specializations in males: the phenomenon that Eberhard (1985) dubbed cryptic female choice.     

Sexual conflict in twins: male co-twins reduce fitness of female Soay sheep

Males and females often have different requirements during early development, leading to sex-specific interactions between developing offspring. In polytocous mammals, competition for limited resources in utero may be asymmetrical between the sexes, and androgens produced by male foetuses could have adverse effects on the development of females, with potentially long-lasting consequences. We show here, in an unmanaged population of Soay sheep, that female lambs with a male co-twin have reduced birth weight relative to those with a female co-twin, while there was no such effect in male twins. In addition, females with a male co-twin had lower lifetime breeding success, which appeared to be mainly driven by differences in first-year survival. These results show that sex-specific sibling interactions can have long-term consequences for survival and reproduction, with potentially important implications for optimal sex allocation.     

High frequency of polyandry in a lek mating system

The adaptive significance of polyandry by female birds in theabsence of direct benefits remains unclear. We determined thefrequencies of polyandrous mating and multiple paternity inthe ruff, a lekking shorebird with a genetic dimorphism inmale mating behavior. More than half of female ruffs mate with, and have clutches fertilized by, more than one male. Individualfemales mate with males of both behavioral morphs more oftenthan expected. Polyandrous mating was more likely followingcopulation interference, but interference was uncommon. Themultiple paternity rate of ruffs is the highest known for avian lekking species and for shorebirds. The general hypothesis thatpair-bond constraints are the major selective factor favoringmultiple mating in birds does not predict our findings. Activegenetic diversification, which has been widely dismissed asa functional explanation for polyandrous mating in birds, mayapply with respect to the behavioral polymorphism in ruffs becauseof a Mendelian genetic basis for male behavioral morph determinationand aspects of male—male cooperation and female choice.However, rates of multiple paternity in other species of lekkingbirds are higher than generally realized, and the potentialbenefits of diversification in general deserve further consideration.